Anterior Swim Bladder Research Articles

Dipole source encoding and tracking by the goldfish auditory system

In goldfish and other otophysans, the Weberian ossicles mechanically link the saccule of the inner ear to the anterior swimbladder chamber (ASB). These structures are correlated with enhanced sound-pressure sensitivity and greater sensitivity at high frequencies (600-2000 Hz). However, surprisingly little is known about the potential impact of the ASB on other otolithic organs and about how auditory responses are modulated by discrete sources that change their location or orientation with respect to the ASB. In this study, saccular and lagenar nerve fiber responses and conditioned behaviors of goldfish were measured to a small, low-frequency (50 Hz) vibrating sphere (dipole) source as a function of its location along the body and its orientation with respect to the ASB. Conditioned behaviors and saccular nerve fiber activity exhibited response characteristics nearly identical to those measured from a hydrophone in the same relative position as the ASB. By contrast, response patterns from lagena fibers could not be predicted by pressure inputs to the ASB. Deflation of the ASB abolished the characteristic spatial response pattern of saccular but not lagena fibers. These results show that: (1) the lagena is not driven by ASB-mediated pressure inputs to the ear; (2) the ASB-saccule pathway dominates behavioral responsiveness, operating effectively at frequencies as low as 50 Hz; and (3) behavioral and neural (saccular) responses are strongly modulated by the position and orientation of the dipole with respect to the ASB.

The ears of butterflyfishes (Chaetodontidae): ‘hearing generalists' on noisy coral reefs?

Analysis of the morphology of all three otolithic organs (sacculus, lagena and utriculus), including macula shape, hair cell morphology, density, orientation pattern, otolith morphology and the spatial relationships of the swimbladder and ear, reveals that butterflyfishes in the genera Chaetodon (which has anterior swimbladder horns) and Forcipiger (which lacks anterior swimbladder horns) both demonstrate the ear morphology typical of teleosts that lack otophysic connections, fishes that have traditionally been considered to be 'hearing generalists'.

Functional morphology of the sonic apparatus in the fawn cusk‐eel Lepophidium profundorum (Gill, 1863)

Recent reports of high frequency sound production by cusk-eels cannot be explained adequately by known mechanisms, i.e., a forced response driven by fast sonic muscles on the swimbladder. Time to complete a contraction-relaxation cycle places a ceiling on frequency and is unlikely to explain sounds with dominant frequencies above 1 kHz. We investigated sonic morphology in the fawn cusk-eel Lepophidium profundorum to determine morphology potentially associated with high frequency sound production and quantified development and sexual dimorphism of sonic structures. Unlike other sonic systems in fishes in which muscle relaxation is caused by internal pressure or swimbladder elasticity, this system utilizes antagonistic pairs of muscles: ventral and intermediate muscles pull the winglike process and swimbladder forward and pivot the neural arch (neural rocker) above the first vertebra backward. This action stretches a fenestra in the swimbladder wall and imparts strain energy to epineural ribs, tendons and ligaments connected to the anterior swimbladder. Relatively short antagonistic dorsal and dorsomedial muscles pull on the neural rocker, releasing strain energy, and use a lever advantage to restore the winglike process and swimbladder to their resting position. Sonic components grow isometrically and are typically larger in males although the tiny intermediate muscles are larger in females. Although external morphology is relatively conservative in ophidiids, sonic morphology is extremely variable within the family.

Acoustic communication in territorial butterflyfish: test of the sound production hypothesis

Butterflyfishes are conspicuous members of coral reefs and well known for their visual displays during social interactions. Members of the genus Chaetodon have a unique peripheral arrangement of the anterior swim bladder that connects with the lateral line (the laterophysic connection) and in many species projects towards the inner ear. This morphology has lead to the proposal that the laterophysic connection and swim bladder system may be a specialized structure for the detection of sound. However, the relevant stimuli, receiver mechanisms and functions for these putative hearing structures were unknown because butterflyfishes were previously not recognized to produce sounds during natural behavior. We performed field experiments to test the hypothesis that Chaetodon produces sounds in natural social contexts. Acoustic and motor behaviors of the monogamous multiband butterflyfish, C. multicinctus, were evoked and recorded by placement of bottled fish into feeding territories of conspecific pairs. We demonstrate that territory defense includes the production of agonistic sounds and hydrodynamic stimuli that are associated with tail slap, jump, pelvic fin flick and dorsal-anal fin erection behaviors. In addition, grunt pulse trains were produced by bottled intruders and are tentatively interpreted to function as an alert call among pair mates. Acoustic behaviors include low frequency hydrodynamic pulses <100 Hz, sounds with peak energy from 100 Hz to 500 Hz, and a broadband high frequency click (peak frequency=3.6 kHz), which is produced only during the tail slap behavior. These results provide a biological framework for future studies to interpret the proximate function of the acoustico-lateralis sensory system, the evolution of the laterophysic mechanism and their relevance to butterflyfish social behavior.

Sound communication by the forceps fish, Forcipiger flavissimus (Chaetodontidae)

The forceps fish, Forcipiger flavissimus (family Chaetodontidae), lacks the anterior swim bladder horns and laterophysic connection that are proposed to improve processing of acoustic signals in the genus Chaetodon. Despite the lack of hearing specializations, laboratory experiments using hydrophones synchronized to video revealed the forceps fish produce at least three sounds: (1) a pulse (21‐ms duration, peak frequency=318 Hz) associated with rapid cranial elevation, (2) a low‐frequency pulse (9‐ms duration, peak frequency=41 Hz) associated with anal fin retraction and elevation, and (3) a high‐frequency broadband click (3‐ms duration, peak frequency=7924 Hz) associated with tail slap behavior. Auditory evoked potential experiments demonstrate that hearing thresholds for this species are 10–21 dB higher than Chaetodon in the 200–600‐Hz band. High‐speed kinematic analyses show that motor movements associated with some acoustic behaviors are different than those in Chaetodon, thus the presence of sound production may be the ancestral state for the family but the mechanisms are divergent. Field observations on Hawaiian reefs reveal that forceps fish occur in pairs and trios that may be haremic, and use acoustic communication among group members.[Work supported by NSF IBN0137883 to TT.]

Acoustico‐lateralis communication in coral reef butterflyfishes

Butterflyfishes are conspicuous members of coral reefs and well known for their pairing behavior and visual displays during social interactions. Members of the genus Chaetodon have a unique arrangement of the anterior swim bladder horns that connect with the lateral line (the laterophysic connection) and also project towards the inner ear, but functions for this putative acoustico‐lateralis adaptation were not known. Field experiments demonstrate that the monogamous multiband butterflyfish, C. multicinctus, produces hydrodynamic pulses and sounds during territorial defense, and pulse trains that may be an alert call to the mate. In field choice tests, individuals could distinguish mates from nonmates and produced different calls to each, thus demonstrating the existence of mate recognition and context‐specific sound production. Laboratory experiments show that sound production differs among sexes, hydrodynamic pulses are of low frequency (<100 Hz), and sounds have peak energy from 100–500 Hz. Auditory evo...

The laterophysic connection and swim bladder of butterflyfishes in the genus Chaetodon (Perciformes: Chaetodontidae)

The laterophysic connection (LC) is an association between bilaterally paired, anterior swim bladder extensions (horns) and medial openings in the supracleithral lateral line canals that diagnoses butterflyfishes in the genus Chaetodon. It has been hypothesized that the LC makes the lateral line system sensitive to sound pressure stimuli that are transmitted by the swim bladder horns and converted to fluid flow into the lateral line system via a laterophysic tympanum. The purpose of this study was to define variation in the morphology of the LC, swim bladder and swim bladder horns among 41 Chaetodon species from all 11 Chaetodon subgenera and a species from each of four non-Chaetodon genera using gross dissection, histological analysis as well as 2D or 3D CT (computed tomographic) imaging of live, anesthetized fishes. Our results demonstrate that the lateral line system appears rather unspecialized with well-ossified narrow canals in all species examined. Two LC types (direct and indirect), defined by whether or not the paired anterior swim bladder horns are in direct contact with a medial opening in the supracleithral lateral line canal, are found among species examined. Two variants on a direct LC and four variants of an indirect LC are defined by combinations of soft tissue anatomy (horn length [long/short] and width [wide/narrow], number of swim bladder chambers [one/two], and presence/absence of mucoid connective tissue in the medial opening in the supracleithrum). The combination of features defining each LC variant is predicted to have functional consequences for the bioacoustics of the system. These findings are consistent with the recent discovery that Chaetodon produce sounds during social interactions. The data presented here provide the comparative morphological context for the functional analysis of this novel swim bladder-lateral line connection.

The laterophysic connection: A novel specialization thought to enhance sound pressure sensitivity in butterflyfishes (Chaetodontidae, Chaetodon)

Morphological specializations that enhance sound reception have been described among fishes, but sources of behaviorally-significant sound stimuli and sound transduction mechanisms are known for very few bony fishes. Butterflyfishes in the genus Chaetodon have a unique sensory specialization, the laterophysic connection (LC), defined anterior swim bladder extensions (horns) in association with medial openings in the lateral line canals of the cranial supracleithral bones. The LC is hypothesized to enhance sensitivity of both the lateral line and ear to sound pressure. Variation in LC morphology among species is defined by variation in soft tissues and is thought to be functionally significant. Preliminary field studies demonstrate that C. multicinctus produces sounds during agonistic interactions, thus providing a source of potentially relevant sound stimuli. Presence of an inflated swim bladder in close proximity to well-developed supracleithral openings in pelagic tholichthys stage individuals (15 mm SL) and horn development at the end of the tholichthys stage (25–29 mm SL) in C. ocellatus suggests that sound may also play an important role in the early life history of Chaetodon. [Work supported by the NSF IBN-9603896 to J.F.W.]

A mathematical analysis of the peripheral auditory system mechanics in the goldfish (Carassius auratus).

The dynamic response of the goldfish peripheral auditory system has been analyzed using lumped-parameter mechanical and fluid system models for the swimbladder, Weberian apparatus, and saccule. The swimbladder is treated as a two degree-of-freedom mechanical system consisting of two coupled mass-spring-damper arrangements. The swimbladder is coupled to the Weberian ossicles using a phenomenological analysis of the anterior swimbladder tunica externa which permits both stretching and sliding. Analysis of the saccule features only a single degree of freedom, corresponding to the direction of orientation of the ciliary bundles. Inputs to the saccule consist of the transverse canal fluid motion and the motion of the animal's head (assumed to match the local acoustic particle motion). Mechanical properties required for the system equations were estimated from published literature, direct measurements, and curve fits to experimental data for the motions of the swimbladders. The results indicate that the Weberian apparatus has a significant impact on hearing ability over the entire auditory bandwidth, not just at higher frequencies, and that the saccule functions as a displacement sensor above approximately 300 Hz.

Sequence, expression and genetic mapping of a rainbow trout retinoblastoma cDNA.

A full-length cDNA for retinoblastoma (RB1) has been cloned from a cDNA library prepared from 3-week-old rainbow trout (Oncorhynchus mykiss) eyed embryos. The trout RB1 cDNA encodes a predicted protein of 910 amino acids and is the most divergent cloned retinoblastoma gene sequence to date. RT-PCR studies reveal high levels of RB1 expression by the second week of embryogenesis, which remains uniformly expressed until hatching. Expression studies of adult fish tissues show the RB1 gene to be expressed in all tissues examined, including the oesophagus, eye, liver, intestine, posterior and anterior kidney, skin, stomach, muscle, spleen, gill, swim bladder, gonads and brain. The RB1 gene appears to be a single copy gene based on Southern analysis, and maps to linkage group XVI in the trout genome map. Polymorphisms in the RB1 gene and in closely linked markers should facilitate LOH analysis of RB1.

A cohesive lumped parameter analysis of the mechanics of the goldfish peripheral auditory system

A mathematical analysis has been formulated to model the dynamic behavior of the goldfish peripheral auditory system, including the swimbladders, Weberian apparatus, and saccule. The two-chambered goldfish swimbladder is treated as a two degree-of-freedom mechanical system consisting of two coupled mass-spring-damper arrangements. The swimbladder is coupled to the Weberian ossicles using a phenomenological analysis of the anterior swimbladder tunica externa which permits both stretching and sliding. Analysis of the saccule features only a single degree-of-freedom, corresponding to the direction of orientation of the ciliary bundles. Inputs to the saccule consist of the transverse canal fluid motion and the motion of the animal’s head (assumed to match the local acoustic particle motion). Mechanical properties required for the system equations were estimated from published literature and direct measurements. Results of the analysis compare favorably to experimental data for the motions of the swimbladders and Weberian ossicles. The results indivate that the Weberian apparatus has a significant impact on the hearing ability over a broad frequency range and that the saccule functions as a displacement sensor above approximately 300 Hz. [Work supported by ONR Grant No. N00014-94-1-0337 and the ASA Hunt Fellowship.]

An experimental study of the peripheral auditory mechanics in the goldfish (Carassius auratus) and oscar (Astronotus ocellatus)

Dynamic mechanical responses of peripheral auditory organs in the goldfish (Carassius auratus), considered a hearing specialist because of its coupling via the Weberian ossicles between the swimbladder and inner ear, and the oscar (Astronotus ocellatus), an auditory nonspecialist, were measured in vivo using a noncontact, noninvasive ultrasonic system. Motion of the auditory organs was induced under water using pure tones at frequencies ranging from 12.5 to 3000 Hz. Measurements were made in both species with swimbladders intact and swimbladders deflated. Results from 23 goldfish and 38 oscars show that the swimbladder controls auditory bandwidth not only in hearing specialists, but also in nonspecialists which have no special coupling between the swimbladder and inner ear. Dual resonances routinely observed in the response of the anterior swimbladder, and motion of the Weberian ossicles transmitted to the saccular otolith at higher frequencies, contribute to the relatively broad auditory bandwidth of the goldfish. Although data were recorded only in the medial-lateral direction, they clearly indicate that displacement of the saccular otolith relative to its sensory epithelium in both the goldfish and oscar correlates with auditory thresholds for these animals reported in the literature. [Work supported by ONR Grant No. N00014-94-1-0337.]